Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species

Abstract

Many metagenomic sequencing studies have observed the presence of closely related bacterial species or genotypes in the same microbiome. Previous attempts to explain these patterns of microdiversity have focused on the abiotic environment, but few have considered how biotic interactions could drive patterns of microbiome diversity. We dissected the patterns, processes, and mechanisms shaping the ecological distributions of three closely related Staphylococcus species in cheese rind biofilms. Paradoxically, the most abundant species (S. equorum) is the slowest colonizer and weakest competitor based on growth and competition assays in the laboratory. Through in vitro community reconstructions, we determined that biotic interactions with neighboring fungi help resolve this paradox. Species-specific stimulation of the poor competitor by fungi of the genus Scopulariopsis allows S. equorum to dominate communities in vitro as it does in situ. Results of comparative genomic and transcriptomic experiments indicate that iron utilization pathways, including a homolog of the S. aureus staphyloferrin B siderophore operon pathway, are potential molecular mechanisms underlying Staphylococcus-Scopulariopsis interactions. Our integrated approach demonstrates that fungi can structure the ecological distributions of closely related bacterial species, and the data highlight the importance of bacterium-fungus interactions in attempts to design and manipulate microbiomes.

Nonconventional starter cultures of coagulase-negative staphylococci to produce animal-derived fermented foods, a SWOT analysis

“…Fungi also contribute to the shaping of the ecological distribution of CNS species in cheese rind communities, possibly by stimulating the dominance of S. equorum over S. saprophyticus and S. xylosus through a molecular mechanism involving iron utilization (Kastman et al . ). In addition, the effects of temperature on CNS growth require consideration (Søndergaard and Stahnke ), as they determine their adaptation to processing (Stavropoulou et al .…”

Extensive Horizontal Gene Transfer in Cheese-Associated Bacteria

“…Horizontally transferred genes are not always expressed in the recipient genome, because of possible incompatibilities in promoter sequence (Ochman et al, 2000). As iron is a limiting resource in cheese (Kastman et al, 2016;Monnet et al, 2012), we reasoned that if RUSTI is a functional operon, it would likely have increased expression in the presence of additional competition for iron. To assess whether RUSTI genes are regulated in the presence of competition, we grew G. arilaitensis JB182 alone or in the presence of Penicillium and performed RNA sequencing (RNA-seq) to monitor gene expression.…”

“…Shotgun metagenomic data from and (Kastman et al, 2016) were assembled with CLC Genomic Workbench 8.0. Representative sequences for ActinoRUSTI or ProteoRUSTI were compared with assembled metagenomes by BLAST.…”

“…We have previously shown that these communities can be used to examine community-based processes, such as succession and interspecies interactions, within an experimentally tractable system Kastman et al, 2016). Given that biofilms such as these are densely populated, and microbes in cheese rinds are under strong selection to obtain limited nutrients (e.g.…”

Genomic insights into the virulence and salt tolerance of Staphylococcus equorum

“…equorum , the genome sequence data of strains KS1039 (GenBank accession: CP013114.1), Mu2 (CAJL00000000.1), UMC-CNS-924 (AVBD00000000.1) and G8HB1 (LAKE00000000.1) published before July 2016 were obtained from the NCBI database (http://ncbi.nlm.nih.gov/genomes). The genome sequence data of 15 strains published after September 2016 were also used for additional comparative genomic analysis 22 . The average nucleotide identity (ANI), which provides a robust measurement of genetic distance among bacterial genomes, among the conserved genes of the genomes was used for comparative analysis 23 .…”